The structural basis for specificity in lipoxygenase catalysis

Protein Science

Volumn 24, Issue 3, 2015, Pages 298-309

  Newcomer, Marcia E ^a   Brash, Alan R ^b  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

arachidonic acid; hydroperoxide oxygenation; linoleic acid; lipoxygenase; oxylipins; polyunsaturated fatty acids

Indexed keywords

HYDROGEN PEROXIDE; LIPOXYGENASE; UNSATURATED FATTY ACID;

ANIMAL; CATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; HUMAN; METABOLISM;

ANIMALS; CATALYSIS; FATTY ACIDS, UNSATURATED; HUMANS; HYDROGEN PEROXIDE; LIPOXYGENASE; MODELS, MOLECULAR; SUBSTRATE SPECIFICITY;

EID: 84938379369     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2626     Document Type: Review

References (52)

1. Ivanov I, Heydeck D, Hofheinz K, Roffeis J, O'Donnell VB, Kuhn H, Walther M, (2010) Molecular enzymology of lipoxygenases. Arch Biochem Biophys 503: 161-174.
2. Samuelsson B, Dahlen SE, Lindgren JA, Rouzer CA, Serhan CN, (1987) Leukotrienes and lipoxins: structures, biosynthesis, and biological effects. Science 237: 1171-1176.
3. Andreou A, Feussner I, (2009) Lipoxygenases-structure and reaction mechanism. Phytochemistry 70: 1504-1510.
4. Zheng Y, Yin H, Boeglin WE, Elias PM, Crumrine D, Beier DR, Brash AR, (2011) Lipoxygenases mediate the effect of essential fatty acid in skin barrier formation: a proposed role in releasing omega-hydroxyceramide for construction of the corneocyte lipid envelope. J Biol Chem 286: 24046-24056.
5. Meyer D, Herrfurth C, Brodhun F, Feussner I, (2013) Degradation of lipoxygenase-derived oxylipins by glyoxysomes from sunflower and cucumber cotyledons. BMC Plant Biol 13: 177.
6. Boutaud O, Aronoff DM, Richardson JH, Marnett LJ, Oates JA, (2002) Determinants of the cellular specificity of acetaminophen as an inhibitor of prostaglandin H(2) synthases. Proc Natl Acad Sci USA 99: 7130-7135.
7. Aronoff DM, Boutaud O, Marnett LJ, Oates JA, (2003) Inhibition of prostaglandin H2 synthases by salicylate is dependent on the oxidative state of the enzymes. J Pharmacol Exp Ther 304: 589-595.
8. Brash AR, (1999) Lipoxygenases: occurrence, functions, catalysis, and acquisition of substrate. J Biol Chem 274: 23679-23682.
9. Andreou A, Brodhun F, Feussner I, (2009) Biosynthesis of oxylipins in non-mammals. Prog Lipid Res 48: 148-170.
10. Hada T, Swift LL, Brash AR, (1997) Discovery of 5R-lipoxygenase activity in oocytes of the surf clam, Spisula solidissima. Biochim Biophys Acta 1346: 109-119.
11. Mortimer M, Jarving R, Brash AR, Samel N, Jarving I, (2006) Identification and characterization of an arachidonate 11R-lipoxygenase. Arch Biochem Biophys 445: 147-155.
12. Brash AR, Schneider C, Hamberg M, (2012) Applications of stereospecifically-labeled fatty acids in oxygenase and desaturase biochemistry. Lipids 47: 101-116.
13. Kuhn H, Sprecher H, Brash AR, (1990) On singular or dual positional specificity of lipoxygenases. The number of chiral products varies with alignment of methylene groups at the active site of the enzyme. J Biol Chem 265: 16300-16305.
14. Sloane DL, Leung R, Craik CS, Sigal E, (1991) A primary determinant for lipoxygenase positional specificity. Nature 354: 149-152.
15. Egmond MR, Vliegenthart JF, Boldingh J, (1972) Stereospecificity of the hydrogen abstraction at carbon atom n-8 in the oxygenation of linoleic acid by lipoxygenases from corn germs and soya beans. Biochem Biophys Res Commun 48: 1055-1060.
16. Coffa G, Imber AN, Maguire BC, Laxmikanthan G, Schneider C, Gaffney BJ, Brash AR, (2005) On the relationships of substrate orientation, hydrogen abstraction, and product stereochemistry in single and double dioxygenations by soybean lipoxygenase-1 and its Ala542Gly mutant. J Biol Chem 280: 38756-38766.
17. Coffa G, Brash AR, (2004) A single active site residue directs oxygenation stereospecificity in lipoxygenases: Stereocontrol is linked to the position of oxygenation. Proc Natl Acad Sci USA [VOL:PAGE #S].
18. Knapp MJ, Seebeck FP, Klinman JP, (2001) Steric control of oxygenation regiochemistry in soybean lipoxygenase-1. J Am Chem Soc 123: 2931-2932.
19. Knapp MJ, Klinman JP, (2003) Kinetic studies of oxygen reactivity in soybean lipoxygenase-1. Biochemistry 42: 11466-11475.
20. Brash AR, Yu Z, Boeglin WE, Schneider C, (2007) The hepoxilin connection in the epidermis. Febs J 274: 3494-3502.
21. Saam J, Ivanov I, Walther M, Holzhutter HG, Kuhn H, (2007) Molecular dioxygen enters the active site of 12/15-lipoxygenase via dynamic oxygen access channels. Proc Natl Acad Sci USA 104: 13319-13324.
22. Schneider C, Pratt DA, Porter NA, Brash AR, (2007) Control of oxygenation in lipoxygenase and cyclooxygenase catalysis. Chem Biol 14: 473-488.
23. Boyington JC, Gaffney BJ, Amzel LM, (1993) The three-dimensional structure of an arachidonic acid 15-lipoxygenase. Science 260: 1482-1486.
24. Garreta A, Val-Moraes SP, Garcia-Fernandez Q, Busquets M, Juan C, Oliver A, Ortiz A, Gaffney BJ, Fita I, Manresa A, Carpena X, (2013) Structure and interaction with phospholipids of a prokaryotic lipoxygenase from Pseudomonas aeruginosa. Faseb J 27: 4811-4821.
25. Minor W, Steczko J, Stec B, Otwinowski Z, Bolin JT, Walter R, Axelrod B, (1996) Crystal structure of soybean lipoxygenase L-1 at 1.4 A resolution. Biochemistry 35: 10687-10701.
26. Skrzypczak-Jankun E, Amzel LM, Kroa BA, Funk MO, (1997) Structure of soybean lipoxygenase L3 and a comparison with its L1 isoenzyme. Proteins 29: 15-31.
27. Youn B, Sellhorn GE, Mirchel RJ, Gaffney BJ, Grimes HD, Kang C, (2006) Crystal structures of vegetative soybean lipoxygenase VLX-B and VLX-D, and comparisons with seed isoforms LOX-1 and LOX-3. Proteins 65: 1008-1020.
28. Gillmor SA, Villasenor A, Fletterick R, Sigal E, Browner MF, (1997) The structure of mammalian 15-lipoxygenase reveals similarity to the lipases and the determinants of substrate specificity [published erratum appears in Nat Struct Biol 1998 Mar;5(3):242]. Nat Struct Biol 4: 1003-1009.
29. Choi J, Chon JK, Kim S, Shin W, (2008) Conformational flexibility in mammalian 15S-lipoxygenase: reinterpretation of the crystallographic data. Proteins 70: 1023-1032.
30. Gilbert NC, Bartlett SG, Waight MT, Neau DB, Boeglin WE, Brash AR, Newcomer ME, (2011) The structure of human 5-lipoxygenase. Science 331: 217-219.
31. Eek P, Jarving R, Jarving I, Gilbert NC, Newcomer ME, Samel N, (2012) Structure of a calcium-dependent 11R-lipoxygenase suggests a mechanism for Ca2+ regulation. J Biol Chem 287: 22377-22386.
32. Xu S, Mueser TC, Marnett LJ, Funk MO, Jr,. (2012) Crystal structure of 12-lipoxygenase catalytic-domain-inhibitor complex identifies a substrate-binding channel for catalysis. Structure 20: 1490-1497.
33. Kobe MJ, Neau DB, Mitchell CE, Bartlett SG, Newcomer ME, (2014) The structure of human 15-lipoxygenase-2 with a substrate mimic. J Biol Chem 289: 8562-8569.
34. Neau DB, Bender G, Boeglin WE, Bartlett SG, Brash AR, Newcomer ME (in press) Crystal Structure of a Lipoxygenase in Complex with Substrate: the arachidonic acid binding site of 8R-lipoxygenase. J Biol Chem 289: 31905-31913.
35. Gaffney BJ, (1996) Lipoxygenases: structural principles and spectroscopy. Annu Rev Biophys Biomol Struct 25: 431-459.
36. Minor W SJ, Stec B, Otwinowski Z, Bolin JT, Walter R, Axelrod B, (1996) Crystal structure of soybean lipoxygenase L-1 at 1.4 A resolution. Biochemistry 35: 10687-10701.
37. Bradshaw MD, Gaffney BJ, (2014) Fluctuations of an exposed pi-helix involved in lipoxygenase substrate recognition. Biochemistry 53: 5102-5110.
38. Gaffney BJ, Bradshaw MD, Frausto SD, Wu F, Freed JH, Borbat P, (2012) Locating a lipid at the portal to the lipoxygenase active site. Biophys J 103: 2134-2144.
39. Gaffney BJ, (2014) Connecting lipoxygenase function to structure by electron paramagnetic resonance. Acc Chem Res 47: 3588-3595.
40. Oldham ML, Brash AR, Newcomer ME, (2005) Insights from the X-ray crystal structure of coral 8R-lipoxygenase: calcium activation via a C2-like domain and a structural basis of product chirality. J Biol Chem 280: 39545-39552.
41. Neau DB, Gilbert NC, Bartlett SG, Boeglin W, Brash AR, Newcomer ME, (2009) The 1.85 A structure of an 8R-lipoxygenase suggests a general model for lipoxygenase product specificity. Biochemistry 48: 7906-7915.
42. Hammarberg T, Provost P, Persson B, Radmark O, (2000) The N-terminal domain of 5-lipoxygenase binds calcium and mediates calcium stimulation of enzyme activity. J Biol Chem 275: 38787-38793.
43. Kulkarni S, Das S, Funk CD, Murray D, Cho W, (2002) Molecular basis of the specific subcellular localization of the C2-like domain of 5-lipoxygenase. J Biol Chem 277: 13167-13174.
44. Ivanov I, Di Venere A, Horn T, Scheerer P, Nicolai E, Stehling S, Richter C, Skrzypczak-Jankun E, Mei G, Maccarrone M, Kuhn H, (2011) Tight association of N-terminal and catalytic subunits of rabbit 12/15-lipoxygenase is important for protein stability and catalytic activity. Biochim Biophys Acta 1811: 1001-1010.
45. Walther M, Hofheinz K, Vogel R, Roffeis J, Kuhn H, (2011) The N-terminal beta-barrel domain of mammalian lipoxygenases including mouse 5-lipoxygenase is not essential for catalytic activity and membrane binding but exhibits regulatory functions. Arch Biochem Biophys 516: 1-9.
46. Hammel M, Walther M, Prassl R, Kuhn H, (2004) Structural flexibility of the N-terminal beta-barrel domain of 15-lipoxygenase-1 probed by small angle X-ray scattering. Functional consequences for activity regulation and membrane binding. J Mol Biol 343: 917-929.
47. Borngraber S, Browner M, Gillmor S, Gerth C, Anton M, Fletterick R, Kuhn H, (1999) Shape and specificity in mammalian 15-lipoxygenase active site. The functional interplay of sequence determinants for the reaction specificity. J Biol Chem 274: 37345-37350.
48. Skrzypczak-Jankun E, Bross RA, Carroll RT, Dunham WR, Funk MO, Jr,. (2001) Three-dimensional structure of a purple lipoxygenase. J Am Chem Soc 123: 10814-10820.
49. de Groot JJ, Garssen GJ, Veldink GA, Vliegenthart JF, Boldingh J, (1975) On the interaction of soybean lipoxygenase-1 and 13-L-hydroperoxylinoleic acid, involving yellow and purple coloured enzyme species. FEBS Lett 56: 50-54.
50. Bushnell EA, Jamil R, Gauld JW, (2013) Gaining insight into the chemistry of lipoxygenases: a computational investigation into the catalytic mechanism of (8R)-lipoxygenase. J Biol Inorg Chem 18: 343-355.
51. Gilbert NC, Rui Z, Neau DB, Waight MT, Bartlett SG, Boeglin WE, Brash AR, Newcomer ME, (2012) Conversion of human 5-lipoxygenase to a 15-lipoxygenase by a point mutation to mimic phosphorylation at Serine-663. FASEB J 26: 3222-3229.
52. Lichtarge O, Sowa ME, (2002) Evolutionary predictions of binding surfaces and interactions. Curr Opin Struct Biol 12: 21-27.